He was a member of the Tennessee House of Representatives from 1829 to 1831 and again from 1835 to 1837, serving each time as Speaker. Upon the resignation from the U.S. Senate of Felix Grundy to accept appointment as United States Attorney General, the Tennessee General Assembly elected Foster his successor. He served in the Senate for the first time from September 17, 1838 to March 4, 1839. The legislature elected him to continue in the new term, but he declined, refusing to take their instruction in how to vote while a Senator; the legislature then turned to Grundy, still Attorney General, to succeed him, which (controversially) Grundy agreed to do.

However, Grundy died in office about a year later. Alfred O. P. Nicholson agreed to serve on an interim basis; then for a period the seat was vacated entirely, but eventually the legislature agreed to elect Foster again to the seat and he agreed to serve. His second period of service in the Senate was from October 17, 1843 to March 4, 1845. During this time he chaired the Senate Committee on Claims. Later in 1845 Foster received the nomination of the Whig party for Governor of Tennessee, but was defeated in the election by Aaron V. Brown of the Democratic Party. Following this, Foster returned to his Nashville law practice until shortly before his death. He is buried in the old City Cemetery in Nashville.

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